The first record of the invasive mosquito species Aedes albopictus in Yemen

Abstract

The invasive mosquito Aedes albopictus is regarded as a public health threat due to its ability to transmit pathogens such as dengue and chikungunya viruses, its wide range of hosts, and its ecological plasticity. Aedes albopictus has already invaded parts of the Middle East region and further expansion is expected. Twenty-two sites in three districts of Yemen (Al Ghaydha, Hawf, and Sayhout) were screened for the presence of mosquitoes. We surveyed water bodies and containers, and deployed Centers for Disease Control and Prevention (CDC) and Biogents Sentinel (BG) traps, spray catches, and aspiration for adult collection. Aedes albopictus was recorded for the first time in Yemen in September 2023, during routine surveillance in Al Mahrah Governorate. Adults and immature stages of Ae. albopictus were identified in Hawf, a city 17 m above sea level in the easternmost part of the Governorate of Al Mahrah, which is located less than 8 km from the border with Oman. Our findings showed that Ae. albopictus adults were coexisting with both Aedesaegypti and Anopheles stephensi in the same location and occupying the same containers with Ae. aegypti with a ratio of 1:2. This is the first report on the presence of Ae. albopictus in Yemen. The proximity, ongoing human activity and transportation exchanges between Al Mahrah and Oman may have played a role in the introduction of this species. Intensive efforts should be undertaken to monitor and manage Ae. albopictus spread in the country, in addition to coordinating cross-border surveillance with Oman. The presence of both Aedes spp. vectors together highlights the need for surveillance for associated diseases and consideration of countermeasures.

Graphical abstract

Highlights

• •First record of Aedes albopictus introduction in Yemen confirming earlier forecasts.
• •Vector-borne disease threat is high due to the coexistence of Ae. albopictus with other dengue and malaria vectors.
• •Areas positioned as points of entry are considered at high risk for the establishment of container-inhabiting Aedes spp.

1. Background

Yemen borders Saudi Arabia and Oman to the north and northeast, respectively. It neighbors Djibouti, Eritrea and Somalia along the Red Sea and Gulf of Aden Maritime borders. The climate is semiarid and arid-tropical with different ecozones (USAID, 2016). Yemen is one of the most water-constrained countries in the Middle East and North Africa, facing a significant risk of drought (USAID, 2016). This risk will in turn reinforce water storage practices among the population, creating suitable habitats for mosquitoes.

Al Mahrah, the easternmost Governorate of Yemen, borders Oman to the east and Hadramout Governorate to the north and west. Hawf District, located in Al Mahrah, harbors a nature reserve that is considered one of the largest forests in the Arabian Peninsula (UNESCO, 2002), with foggy weather and an ascending altitude reaching 1400 m above sea level.

Yemen has a long history of dengue and chikungunya outbreaks (Bin Ghouth et al., 2012; Zayed et al., 2012; Madani et al., 2013; Malik et al., 2014; Rezza et al., 2014; Al-Garadi, 2015; Saied et al., 2015; Saghir et al., 2022), in addition to several unpublished reports. Unrest in the country and successive civil wars amplified the frequency and spread of dengue (Saghir et al., 2022), with overall challenges in the required surveillance and health services (Saied et al., 2015). The main dengue vector in Yemen is Aedes aegypti (Bin Ghouth et al., 2012; Zayed et al., 2012), as well as in the rest of neighboring Saudi Arabia (Naeem et al., 2016; Alahmed et al., 2019). Recently, the introduction of Aedes albopictus in Oman has been announced (Al-Abri et al., 2020; Al Awaidy et al., 2022). According to a recent review, Ae. albopictus has not been recorded in Saudi Arabia (Dawah et al., 2023). A similar species, Aedes unilineatus, which can be misidentified as Ae. albopictus has been reported in Saudi Arabia (Godsey et al., 2003) and Iran (Yaghoobi-Ershadi et al., 2017). Closeness, continuous traffic between Al Mahrah Governorate and Oman, and the transportation of goods may facilitate vector movements and distribution.

Here, we report the first record of Ae. albopictus in Yemen and discuss the factors that may contribute to an increased risk of further spread in the country.

2. Materials and methods

As part of the routine surveillance in 9 southern governorates in Yemen, we conducted mosquito surveillance in Al Mahrah Governorate in 2023. We inspected 22 sites in Al Mahrah: 9 in Al Ghaydha, 6 in Hawf, and 7 in Sayhout districts, with the respective average elevation of 17 m, 17 m, and 8 m above sea level, respectively. We ran 5-day indoor inspections, outdoor field surveillance, and checked the surrounding water bodies and containers in each site. For adult collections, Centers for Disease Control and Prevention (CDC) and Biogents Sentinel (BG) traps, spray catches and aspiration were employed (Fig. 1). Larvae were collected and reared to the adult stage in emergence chambers for confirmatory identification according to the key of Rueda (2004). To avoid misidentification between Ae. albopictus and Ae. unilineatus, we used the keys of Huang (2004) and Dawah et al. (2023).

Fig. 1.

Indoor and outdoor mosquito collections in Al Mahrah Governorate. A Cement basin. B Plastic barrel. C, D Spray catches. E BG traps. F Rearing field-collected larvae to adults.

3. Results

Water bodies and containers were inspected for larvae in Al Mahrah Governorate in 18 out of the 22 sites. A total of 1390 Aedes spp. larvae were collected, 800 of which were from Sayhout, 540 from Hawf, and 50 from Al Ghaydha sites (Table 1). Females without scutal round pale spots and having dark mid-femora with pale apical patches were identified as Ae. albopictus. Emerged adults identified as Ae. albopictus were collected from containers in one spot in Hawf (Site H6: 16°38′08.0″N, 53°02′03.3″E; water temperature of 38 °C) together with Ae. aegypti larvae. The ratio of the emerged adults of Ae. albopictus to Ae. aegypti was 1:2. Most of the breeding containers (83%) were plastic barrels used for water storage and the remaining were cement basins (Fig. 1).

Table 1.

Number of mosquito specimens collected in the inspected districts of Al Mahrah Governorate, Yemen, in 2023–2024 with the confirmed positive sites for Aedes albopictus.

District	Site ID	Collection	Aedes spp. larvae	Emerged adults		Indoor adults		An. stephensi larvae
				Ae. albopictus	Ae. aegypti	Ae. albopictus	Ae. aegypti
Hawf	H1	I & O	40–49
	H2	I & O	150–159		74 (35♀)		1	50–59
	H3	I & O	80–89		38 (17♀)			30–39
	H4	I & O	70–79		29 (13♀)			50–59
	H5	I & O				2	5	80–85
	H6	I & O	200–209	16 (7♀)	32 (15♀)
Al Ghaydha	Gh1	I
	Gh2	I
	Gh3	I
	Gh4	I & O						30–39
	Gh5	I & O						180–189
	Gh6	O	50–59		10 (8♀)			130–139
	Gh7	O						150–159
	Gh8	O						90–99
	Gh9	O						60–69
Sayhut	S1	I & O					2	20–29
	S2	I & O						25
	S3	I & O						22
	S4	I & O					1	30–39
	S5	O	750–759		114 (78♀)			190–199
	S6	I & O	50–59		13 (10♀)			653
	S7	I					1

Abbreviations: I, indoor collection; O, outdoor collection.

On conducting the indoor inspections in the surrounding premises (17 sites), we collected two Ae. albopictus females (Table 1, Fig. 2) together with Ae. aegypti and Anopheles stephensi females. The location positive for adult Ae. albopictus was 100 m away from the larval breeding site in Hawf (Site H5: 16°38′06.0″N, 53°02′01.0″E). We did not find Ae. albopictus in the rest of the sites and locations in Hawf, Al Ghaydhah or Sayhout.

Fig. 2.

A Surveillance sites in Al Mahrah showing the Ae. albopictus-positive site in Hawf (red star). B Adults of Ae. albopictus from both indoor collections of adults and emerged reared adults.

4. Discussion

The geographical location, environmental and socioeconomic factors in Yemen have demonstrated suitability to Ae. aegypti abundance and its associated dengue and chikungunya outbreaks. Dickens et al. (2018) identified areas of high suitability for Ae. albopictus that overlapped with those suitable for Ae. aegypti in the coastal areas of the Middle East. The Middle East areas of suitability in their maps included the Indian Ocean coastline of Yemen and Oman. This is consistent with our findings in Yemen and the earlier introduction of Ae. albopictus in Oman (Al-Abri et al., 2020; Al Awaidy et al., 2022). At the northern borders of Yemen, there was an anticipated scenario of Ae. albopictus introduction into Saudi Arabia after its establishment in Lebanon, Syria (Haddad et al., 2007) and Jordan (Kanani et al., 2017). However, Ae. albopictus has not yet been recorded in Saudi Arabia (Dawah et al., 2023).

The proximity of Hawf to Oman border positions the area as a point of entry with a maximum risk of Aedes spp. establishment, as discussed by Ducheyne et al. (2018). Frequent human and trade movements may have exacerbated the likelihood of importing Ae. albopictus to the specific locations across the borders. Dickens et al. (2018) highlighted the role of transportation in globalization and urban spread in introducing Aedes spp.

According to our monthly monitoring, the Ae. albopictus population is not yet widely established in the Al Mahrah Governorate nor in the neighboring sites in Yemen. Nevertheless, due to the environmental suitability, potential invasion toward areas in the Southwest of Yemen, parallel to the Gulf of Aden and the Red Sea coast, is highly anticipated according to the maps and study of Kamal et al. (2018). Minimum temperatures, absolute humidity, and accessibility to the human population were considered key factors for the presence of both Ae. aegypti and Ae. albopictus (Dickens et al., 2018). The presence of nearby large water surface upsurging the absolute humidity (Dickens et al., 2018), together with the foggy atmosphere and the elevation above sea level (CBD, 2024), provide suitable environments for the occurrence of both species of Aedes in Hawf.

The predicted probability of Ae. albopictus presence in the Eastern Mediterranean Region (EMR) forecasted Yemen, among other countries, as a suitable region with high risk of establishment (Ducheyne et al., 2018). Climatic and demographic factors were identified as key determinants of Ae. albopictus establishment and emphasized the importance of precipitation as a limiting factor in the arid EMR (Ducheyne et al., 2018). Our results highlight the accuracy of forecasts predicting a high likelihood of Ae. albopictus introduction in Yemen.

5. Conclusions

We are documenting the first report on the presence of Ae. albopictus in Yemen. Proximity and movement between Al Mahrah and Oman may have played a role in the introduction of the vector. The presence of both Aedes spp. vectors in this area accentuates the need for disease surveillance and meticulous countermeasures in synergy with Oman. In coordination with health authorities, we are intensifying the surveillance efforts near the borders of Al Mahrah Governorate and in other suspected areas to monitor the spread of the invasive species of Aedes. This will support Yemen’s efforts in limiting the establishment of the vector population and increase the efficiency of the commenced control measures.

Ethical approval

Not applicable.

CRediT authorship contribution statement

Alia Zayed: Conceptualization, Visualization, Methodology, Validation, Writing - original draft, Writing - review & editing. Yasser Baheshm: Visualization, Supervision, Writing - review & editing. Mohammed Al Amoudi: Data curation, Investigation, Validation. Salim Bin Shabiz: Methodology, Investigation. Matthew Jensen Montgomery: Conceptualization, Visualization, Writing - review and editing.

Data availability

The data supporting the conclusions of this article are included within the article.

Disclaimer

Some authors are military service members or federal employee of the United States government. This work was prepared as part of their official duties. Title 17 U.S.C. 105 provides that “copyright protection under this title is not available for any work of the United States Government.” Title 17 U.S.C. 101 defines a U.S. Government work as work prepared by a military service member or employee of the U.S. Government as part of that person’s official duties. The views expressed in this article reflect the results of research conducted by the author and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense, nor the United States Government.

Funding

This study was supported by the Armed Forces Health Surveillance Division, Global Emerging Infections Surveillance Branch (GEIS) under grant ProMIS ID P0041_22_N3 & P0036_23_N3.

Declaration of competing interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.